Methodological challenges and solutions in auditory functional magnetic resonance imaging

Frontiers in Neuroscience

Volumn , Issue 8 JUL, 2014, Pages

  Peelle, Jonathan E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Auditory cortex; Auditory perception; Executive function; Hearing; Music; Speech

Indexed keywords

ARTICLE; AUDITORY CORTEX; AUDITORY NERVOUS SYSTEM; AUDITORY STIMULATION; AUDITORY SYSTEM; CARDIAC GATED IMAGING; COGNITION; ECHO PLANAR IMAGING; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; NOISE REDUCTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; ACOUSTIC NOISE; ANTERIOR CINGULATE; AUDITORY MASKING; AUDITORY RESPONSE; BOLD SIGNAL; COMPREHENSION; EAR PROTECTION; ELECTROCORTICOGRAPHY; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; ENERGETIC MASKING; EPISODIC MEMORY; EXECUTIVE FUNCTION; FLUORESCENCE IMAGING; FORCE; FUNCTIONAL NEUROIMAGING; HEARING; HEARING IMPAIRMENT; HEMODYNAMICS; IMAGE QUALITY; IMAGING AND DISPLAY; INSULA; INTERLEAVED SILENT STEADY STATE IMAGING; LORENTZ FORCE; LOUDNESS; MAGNETIC FIELD; MAGNETOENCELPHALOGRAPHY; NERVE POTENTIAL; NOISE; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIMARY AUDITORY CORTEX; RADIOFREQUENCY; REVIEW; SECONDARY AUDITORY CORTEX; SIGNAL NOISE RATIO; SOUND INTENSITY; SPARSE IMAGING; SPEECH; STEADY STATE; TEMPORAL RESOLUTION; WORKING MEMORY;

EID: 84905898806     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00253     Document Type: Article

References (99)

1. Adank, P. (2012). The neural bases of difficult speech comprehension and speech production: Two Activation Likelihood Estimation (ALE) meta-analyses. Brain Lang 122, 42-54.
2. Aguirre, G. K., Zarahn, E. and D'Esposito, M. (1998). The variability of human, BOLD hemodynamic responses. NeuroImage 8, 360-369.
3. Amaro, J., Edson, Williams, S. C. R., Shergill, S. S., Fu, C. H. Y., MacSweeney, M., Picchioni, M. M., Brammer, M. J. and McGuire, P. K. (2002). Acoustic noise and functional magnetic resonance imaging: Current strategies and future prospects. J Magn Reson Imaging 16, 497-510.
4. Bandettini, P. A., Jesmanowicz, A., Van Kylen, J., Birn, R. M. and Hyde, J. S. (1998). Functional MRI of brain activation induced by scanner acoustic noise. Magnet Reson Med 39, 410-416.
5. Bekinschtein, T. A., Davis, M. H., Rodd, J. M. and Owen, A. M. (2011). Why clowns taste funny: The relationship between humor and semantic ambiguity. J Neurosci 31, 9665-9671.
6. Belin, P., Zatorre, R. J., Hoge, R., Evans, A. C. and Pike, B. (1999). Event-related fMRI of the auditory cortex. NeuroImage 10, 417-429.
7. Besser, J., Zekveld, A. A., Kramer, S. E., Rönnberg, J. and Festen, J. M. (2012). New measures of masked text recognition in relation to speech-in-noise perception and their associations with age and cognitive abilities. J Speech Lang Hear Res 55, 194-209.
8. Brown, T. A., Joanisse, M. F., Gati, J. S., Hughes, S. M., Nixon, P. L., Menon, R. S. and Lomber, S. G. (2013). Characterization of the blood-oxygen level-dependent (BOLD) response in cat auditory cortex using high-field fMRI. NeuroImage 64, 458-465.
9. Chambers, J., Akeroyd, M. A., Summerfield, A. Q. and Palmer, A. R. (2001). Active control of the volume acquisition noise in functional magnetic resonance imaging: Method and psychoacoustical evaluation. J Acoust Soc Am 110, 3041-3054.
10. Chambers, J., Bullock, D., Kahana, Y., Kots, A. and Palmer, A. (2007). Developments in active noise control sound systems for magnetic resonance imaging. Appl Acoust 68, 281-295.
11. Cho, Z.-H., Chung, S.-C., Lim, D.-W. and Wong, E. K. (1998a). Effects of the acoustic noise of the gradient systems on fMRI: A study on auditory, motor, and visual cortices. Magn Reson Med 39, 331-335.
12. Cho, Z.-H., Chung, S. T., Chung, J. Y., Park, S. H., Kim, J. S., Moon, C. H. and Hong, I. K. (1998b). A new silent magnetic resonance imaging using a rotating DC gradient. Magn Reson Med 39, 317-321.
13. Cousins, K. A. Q., Dar, H., Wingfield, A. and Miller, P. (2014). Acoustic masking disrupts timedependent mechanisms of memory encoding in word-list recall. Mem Cogn 42, 622-638.
14. Cusack, R., Cumming, N., Bor, D., Norris, D. and Lyzenga, J. (2005). Automated post-hoc noise cancellation tool for audio recordings acquired in an MRI scanner. Hum Brain Mapp 24, 299-304.
15. Davis, M. H., Ford, M. A., Kherif, F. and Johnsrude, I. S. (2011). Does semantic context benefit speech understanding through "top-down" processes? Evidence from time-resolved sparse fMRI. J Cognitive Neurosci 23, 3914-3932.
16. Davis, M. H. and Johnsrude, I. S. (2003). Hierarchical processing in spoken language comprehension. J Neurosci 23, 3423-3431.
17. Davis, M. H. and Johnsrude, I. S. (2007). Hearing speech sounds: Top-down influences on the interface between audition and speech perception. Hear Res 229, 132-147.
18. Doehrmann, O., Naumer, M. J., Volz, S., Kaiser, J. and Altmann, C. F. (2008). Probing category selectivity for environmental sounds in the human auditory brain. Neuropsychologia 46, 2776-2786.
19. Doehrmann, O., Weigelt, S., Altmann, C. F., Kaiser, J. and Naumer, M. J. (2010). Audiovisual functional magnetic resonance imaging adaptation reveals multisensory integration effects in object-related sensory cortices. J Neurosci 30, 3370-3379.
20. Dosenbach, N. U. F., Fair, D. A., Cohen, A. L., Schlaggar, B. L. and Petersen, S. E. (2008). A dual-networks architecture of top-down control. Trends Cognit Sci 12, 99-105.
21. Eckert, M. A., Menon, V., Walczak, A., Ahlstrom, J., Denslow, S., Horwitz, A. and Dubno, J. R. (2009). At the heart of the ventral attention system: The right anterior insula. Hum Brain Mapp 30, 2530-2541.
22. Edelstein, W. A., Hedeen, R. A., Mallozzi, R. P., El-Hamamsy, S.-A., Ackermann, R. A. and Havens, T. J. (2002). Making MRI quieter. Magn Reson Imaging 20, 155-163.
23. Eden, G. F., Joseph, J. E., Brown, H. E., Brown, C. P. and Zeffiro, T. A. (1999). Utilizing hemodynamic delay and dispersion to detect fMRI signal change without auditory interference: The behavior interleaved gradients technique. Magn Reson Med 41, 13-20.
24. Edmister, W. B., Talavage, T. M., Ledden, P. J. and Weisskoff, R. M. (1999). Improved auditory cortex imaging using clustered volume acquisitions. Hum Brain Mapp 7, 89-97.
25. Elliott, M. R., Bowtell, R. W. and Morris, P. G. (1999). The effect of scanner sound in visual, motor, and auditory functional MRI. Magnet Reson Med 41, 1230-1235.
26. Engel, A. and Keller, P. E. (2011). The perception of musical spontaneity in improvised and imitated jazz performances. Front Psychol 2, 83.
27. Erb, J., Henry, M. J., Eisner, F. and Obleser, J. (2013). The brain dynamics of rapid perceptual adaptation to adverse listening conditions. J Neurosci 33, 10688-10697.
28. Foster, J. R., Hall, D. A., Summerfield, A. Q., Palmer, A. R. and Bowtell, R. W. (2000). Soundlevel measurements and calculations of safe noise dosage during EPI at 3 T. J Magn Reson Imaging 12, 157-163.
29. Gaab, N., Gabrieli, J. D. E. and Glover, G. H. (2007). Assessing the influence of scanner background noise on auditory processing. II. An fMRI study comparing auditory processing in the absence and presence of recorded scanner noise using a sparse design. Hum Brain Mapp 28, 721-732.
30. Guimaraes, A. R., Melcher, J. R., Talavage, T. M., Baker, J. R., Ledden, P. J., Rosen, B. R., Kiang, N. Y. S., Fullerton, B. C. and Weisskoff, R. M. (1998). Imaging subcortical auditory activity in humans. Hum Brain Mapp 6, 33-41.
31. Hall, A. J., Brown, T. A., Grahn, J. A., Gati, J. S., Nixon, P. L., Hughes, S. M., Menon, R. S. and Lomber, S. G. (2014). There's more than one way to scan a cat: Imaging cat auditory cortex with high-field fMRI using continuous or sparse sampling. J Neurosci Meth 224, 96-106.
32. Hall, D. A., Chambers, J., Akeroyd, M. A. and Foster, J. R. (2009). Acoustic, psychophysical, and neuroimaging measurements of the effectiveness of active cancellation during auditory functional magnetic resonance imaging. J Acoust Soc Am 125, 347-359.
33. Hall, D. A., Haggard, M. P., Akeroyd, M. A., Palmer, A. R., Summerfield, A. Q., Elliott, M. R., Gurney, E. M. and Bowtell, R. W. (1999). "Sparse" temporal sampling in auditory fMRI. Hum Brain Mapp 7, 213-223.
34. Hall, D. A., Summerfield, A. Q., Gonçalves, M. S., Foster, J. R., Palmer, A. R. and Bowtell, R.W. (2000). Time-course of the auditory BOLD response to scanner noise. Magnet Reson Med 43, 601-606.
35. Haller, S., Bartsch, A. J., Radue, E. W., Klarhöfer, M., Seifritz, E. and Scheffler, K. (2005). Effect of fMRI acoustic noise on non-auditory working memory task: comparison between continuous and pulsed sound emitting EPI. Magn Reson Mater Phy 18, 263-271.
36. Haller, S., Hornola, G. A., Scheffler, K., Beckmann, C. F. and Bartsch, A. J. (2009). Background MR gradient noise and non-auditory BOLD activations: A data-driven perspective. Brain Res 1282, 74-83.
37. Harms, M. P. and Melcher, J. R. (2002). Sound repetition rate in the human auditory pathway: Representations in the waveshape and amplitude of fMRI activation. J Neurophysiol 88, 1433-1450.
38. Heinrich, A. and Schneider, B. A. (2011). Elucidating the effects of ageing on remembering perceptually distorted word pairs. Q J Exp Psychol 64, 186-205.
39. Hennel, F., Girard, F. and Loenneker, T. (1999). "Silent" MRI with soft gradient pulses. Magnet Reson Med 42, 6-10.
40. Hommel, B., Fischer, R., Colzato, L. S., van den Wildenberg, W. P. M. and Cellini, C. (2012). The effect of fMRI (noise) on cognitive control. J Exp Psychol Human 38, 290-301.
41. Junqua, J.-C. (1996). The influence of acoustics on speech production: A noise-induced stress phenomenon known as the Lombard reflex. Speech Comm 20, 13-22.
42. Katsunuma, A., Takamori, H., Sakakura, Y., Hamamura, Y., Ogo, Y. and Katayama, R. (2001). Quiet MRI with novel acoustic noise reduction. Magn Reson Mater Phy 13, 139-144.
43. Kuchinsky, S. E., Ahlstrom, J. B., Vaden Jr., K. I., Cute, S. L., Humes, L. E., Dubno, J. R. and Eckert, M. A. (2013). Pupil size varies with word listening and response selection difficulty in older adults with hearing loss. Psychophysiol 50, 23-34.
44. Langers, D. R. M. and van Dijk, P. (2012). Mapping the tonotopic organization oin human auditory cortex with minimally salient acoustic stimulation. Cereb Cortex 22, 2024-2038.
45. Langers, D. R. M., van Dijk, P. and Backes, W. H. (2005). Interactions between hemodynamic responses to scanner acoustic noise and auditory stimuli in functional magnetic resonance imaging. Magnet Reson Med 53, 49-60.
46. Lash, A., Rogers, C. S., Zoller, A. and Wingfield, A. (2013). Expectation and entropy in spoken word recognition: Effects of age and hearing acuity. Exp Aging Res 39, 235-253.
47. Li, M., Rudd, B., Lim, T. C. and Lee, J.-H. (2011). In situ active control of noise in a 4 T MRI scanner. J Magn Reson Im 34, 662-669.
48. Loenneker, T., Hennel, F., Ludwig, U. and Hennig, J. (2001). Silent BOLD imaging. Magn Reson Mater Phy 13, 76-81.
49. Mansfield, P. and Haywood, B. (2000). Principles of active acoustic control in gradient coil design. Magn Reson Mater Phy 10, 147-151.
50. Mazard, A., Bazoyer, B., Etard, O., Tzourio-Mazoyer, N., Kossyln, S. M. and Mellet, E. (2002). Impact of fMRI acoustic noise on the functional anatomy of visual mental imagery. J Cognitive Neurosci 14, 172-186.
51. McCoy, S. L., Tun, P. A., Cox, L. C., Colangelo, M., Stewart, R. and Wingfield, A. (2005). Hearing loss and perceptual effort: Downstream effects on older adults' memory for speech. Q J Exp Psychol 58, 22-33.
52. Meléndez, J. C. and McCrank, E. (1993). Anxiety-related reactions associated with magnetic resonance imaging examinations. JAMA 270, 745-747.
53. Miller, P. and Wingfield, A. (2010). Distinct effects of perceptual quality on auditory word recognition, memory formation and recall in a neural model of sequential memory. Front Syst Neurosci 4, 14.
54. Moelker, A. and Pattynama, P. M. T. (2003). Acoustic noise concerns in functional magnetic resonance imaging. Hum Brain Mapp 20, 123-141.
55. Moelker, A., Wielopolski, P. A. and Pattynama, P. M. T. (2003). Relationship between magnetic field strength and magnetic-resonance-related acoustic noise levels. Magn Reson Mater Phy 16, 52-55.
56. Mueller, K., Mildner, T., Fritz, T., Lepsien, J., Schwarzbauer, C., Schroeter, M. L. and Möller, H. E. (2011). Investigating brain response to music: A comparison of different fMRI acquisition schemes. NeuroImage 54, 337-343.
57. Murphy, D. R., Craik, F. I. M., Li, K. Z. H. and Schneider, B. A. (2000). Comparing the effects of aging and background noise on short-term memory performance. 15, 323-334.
58. Obleser, J. and Kotz, S. A. (2010). Expectancy constraints in degraded speech modulate the language comprehension network. Cereb Cortex 20, 633-640.
59. Obleser, J., Wise, R. J. S., Dresner, M. A. and Scott, S. K. (2007). Functional integration across brain regions improves speech perception under adverse listening conditions. J Neurosci 27, 2283-2289.
60. Overath, T., Zhang, Y., Sanes, D. H. and Poeppel, D. (2012). Sensitivity to temporal modulation rate and spectral bandwidth in the human auditory system: fMRI evidence. J Neurophysiol 107, 2042-2056.
61. Peelle, J. E. and Davis, M. H. (2012). Neural oscillations carry speech rhythm through to comprehension. Front Psychology 3, 320.
62. Peelle, J. E., Eason, R. J., Schmitter, S., Schwarzbauer, C. and Davis, M. H. (2010a). Evaluating an acoustically quiet EPI sequence for use in fMRI studies of speech and auditory processing. NeuroImage 52, 1410-1419.
63. Peelle, J. E., Johnsrude, I. S. and Davis, M. H. (2010b). Hierarchical processing for speech in human auditory cortex and beyond. Front Hum Neurosci 4, 51.
64. Perrachione, T. K. and Ghosh, S. S. (2013). Optimized design and analysis of sparse-sampling fMRI experiments. Front Neurosci 7, 55.
65. Petkov, C. I., Kayser, C., Augath, M. and Logothetis, N. K. (2009). Optimizing the imaging of the monkey auditory cortex: sparse vs. continuous fMRI. Magn Reson Imaging 27, 1065-1073.
66. Pichora-Fuller, M. K., Schneider, B. A. and Daneman, M. (1995). How young and old adults listen to and remember speech in noise. J Acoust Soc Am 97, 593-608.
67. Price, D. L., De Wilde, J. P., Papadaki, A. M., Curran, J. S. and Kitney, R. I. (2001). Investigation of acoustic noise on 15 MRI scanners from 0.2 T to 3 T. J Magn Reson Imaging 13, 288-293.
68. Pripfl, J., Robinson, S., Leodolter, U., Moser, E. and Bauer, H. (2006). EEG reveals the effect of fMRI scanner noise on noise-sensitive subjects. NeuroImage 31, 332-341.
69. Quirk, M., Letendre, A., Cliottone, R. and Lingley, J. (1989). Anxiety in patients undergoing MR imaging. Radiology 170, 463-466.
70. Rabbitt, P. M. A. (1968). Channel capacity, intelligibility and immediate memory. Q J Exp Psychol 20, 241-248.
71. Ravicz, M. E. and Melcher, J. R. (2001). Isolating the auditory system from acoustic noise during functional magnetic resonance imaging: Examination of noise conduction through the ear canal, head, and body. J Acoust Soc Am 109, 216-231.
72. Ravicz, M. E., Melcher, J. R. and Kiang, N. Y.-S. (2000). Acoustic noise during functional magnetic resonance imaging. J Acoust Soc Am 108, 1683-1696.
73. Robson, M. D., Dorosz, J. L. and Gore, J. C. (1998). Measurements of the temporal fMRI response of the human auditory cortex to trains of tones. NeuroImage 7, 185-198.
74. Rodd, J. M., Johnsrude, I. S. and Davis, M. H. (2012). Dissociating frontotemporal contributions to semantic ambiguity resolution in spoken sentences. Cereb Cortex 22, 1761-1773.
75. Rönnberg, J., Lunner, T., Zekveld, A., Sörqvist, P., Danielsson, H., Lyxell, B., Dahlström, ö., Signoret, C., Stenfelt, S., Pichora-Fuller, M. K. and Rudner, M. (2013). The ease of language understanding (ELU) model: theoretical, empirical, and clinical advances. Front Sys Neurosci 7, 31.
76. Scheffler, K., Bilecen, D., Schmid, N., Tschopp, K. and Seelig, J. (1998). Auditory cortical responses in hearing subjects and unilateral deaf patients as detected by functional magnetic resonance imaging. Cereb Cortex 8, 156-163.
77. Schmitter, S., Diesch, E., Amann, M., Kroll, A., Moayer, M. and Schad, L. R. (2008). Silent echo-planar imaging for auditory FMRI. Magn Reson Mater Phy 21, 317-325.
78. Schwarzbauer, C., Davis, M. H., Rodd, J. M. and Johnsrude, I. (2006). Interleaved silent steady state (ISSS) imaging: A new sparse imaging method applied to auditory fMRI. NeuroImage 29, 774-782.
79. Scott, S. K. and McGettigan, C. (2013). The neural processing of masked speech. Hear Res 303, 58-66.
80. Seifritz, E., Di Salle, F., Esposito, F., Herdener, M., Neuhoff, J. G. and Scheffler, K. (2006). Enhancing BOLD response in the auditory system by neurophysiologically tuned fMRI sequence. NeuroImage 29, 1013-1022.
81. Shah, N. J., Jäncke, L., Grosse-Ruyken, M.-L. and Müller-Gärtner, H.-W. (1999). Influence of acoustic masking noise in fMRI of the auditory cortex during phonetic discrimination. J Magn Reson Im 9, 19-25.
82. Shannon, R. V., Zeng, F.-G., Kamath, V., Wygonski, J. and Ekelid, M. (1995). Speech recognition with primarily temporal cues. Science 270, 303-304.
83. Skouras, S., Gray, M., Critchley, H. and Koelsch, S. (2013). fMRI scanner noise interaction with affective neural processes. PLoS One 8, e80564.
84. Sohoglu, E., Peelle, J. E., Carlyon, R. P. and Davis, M. H. (2012). Predictive top-down integration of prior knowledge during speech perception. J Neurosci 32, 8443-8453.
85. Surprenant, A. M. (1999). The effect of noise on memory for spoken syllables. Int J Psychol 34, 328-333.
86. Talavage, T. M. and Edmister, W. B. (2004). Nonlinearity of fMRI responses in human auditory cortex. Hum Brain Mapp 22, 216-228.
87. Talavage, T. M., Edmister, W. B., Ledden, P. J. and Weisskoff, R. M. (1999). Quantitative assessment of auditory cortex responses induced by imager acoustic noise. Hum Brain Mapp 7, 79-88.
88. Talavage, T. M., Gonzalez-Castillo, J. and Scott, S. K. (2014). Auditory neuroimaging with fMRI and PET. Hear Res 307, 4-15.
89. Talavage, T. M. and Hall, D. A. (2012). How challenges in auditory fMRI led to general advancements for the field. NeuroImage 62, 641-647.
90. Tomasi, D., Caparelli, E. C., Chang, L. and Ernst, T. (2005). fMRI-acoustic noise alters brain activation during working memory tasks. NeuroImage 27, 377-386.
91. Tun, P. A., Benichov, J. and Wingfield, A. (2010). Response latencies in auditory sentence comprehension: Effects of linguistic versus perceptual challenge. Psych Aging 25, 730-735.
92. Vaden, K. I. J., Kuchinsky, S. E., Cute, S. L., Ahlstrom, J. B., Dubno, J. R. and Eckert, M. A. (2013). The cingulo-opercular network provides word-recognition benefit. J Neurosci 33, 18979-18986.
93. Van Engen, K. J., Chandrasekaran, B. and Smiljanic, R. (2012). Effects of speech clarity on recognition memory for spoken sentences. PLoS One 7, e43753.
94. Van Gerven, P. W. M., Vos, H., Van Boxtel, M. P. J., Janssen, S. A. and Miedema, H. M. E. (2009). Annoyance from environmental noise across the lifespan. J Acoust Soc Am 126, 187-194.
95. Wild, C. J., Yusuf, A., Wilson, D., Peelle, J. E., Davis, M. H. and Johnsrude, I. S. (2012). Effortful listening: The processing of degraded speech depends critically on attention. J Neurosci 32, 14010-14021.
96. Wingfield, A., Tun, P. A. and McCoy, S. L. (2005). Hearing loss in older adulthood: What it is and how it interacts with cognitive performance. Curr Dir Psychol Sci 14, 144-148.
97. Yoo, S., Chung, J.-Y., Jeon, H.-A., Lee, K.-M., Kim, Y.-B. and Cho, Z.-H. (2012). Dual routes for verbal repetition: Articulation-based and acoustic-phonetic codes for pseudoword and word repetition, respectively. Brain Lang 122, 1-10.
98. Zekveld, A. A., George, E. L. J., Kramer, S. E., Goverts, S. T. and Houtgast, T. (2007). The development of the text reception threshold test: A visual analogue of the speech reception threshold test. J Speech Lang Hear Res 50, 576-584.
99. Zekveld, A. A. and Kramer, S. E. (2014). Cognitive processing load across a wide range of listening conditions: Insights from pupillometry. Psychophysiol 51, 277-284.